Endocannabinoids regulate the migration of subventricular zone-derived neuroblasts in the postnatal brain

Journal of Neuroscience

Volumn 31, Issue 11, 2011, Pages 4000-4011

  Oudin, Madeleine J ^a   Gajendra, Sangeetha ^a   Williams, Gareth ^a   Hobbs, Carl ^a   Lalli, Giovanna ^a   Doherty, Patrick ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID 2 RECEPTOR ANTAGONIST; CANNABINOID RECEPTOR ANTAGONIST; ENDOCANNABINOID; GREEN FLUORESCENT PROTEIN; LIPOPROTEIN LIPASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME SYNTHESIS; EXPLANT; FEMALE; IN VIVO STUDY; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SUBVENTRICULAR ZONE; TIME LAPSE IMAGING;

ANIMALS; ANIMALS, NEWBORN; ARACHIDONIC ACIDS; BRAIN; CELL LINE; CELL MOVEMENT; CELLS, CULTURED; ENDOCANNABINOIDS; FEMALE; GLYCERIDES; IMMUNOHISTOCHEMISTRY; LIPOPROTEIN LIPASE; MALE; MICE; MONOACYLGLYCEROL LIPASES; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RECEPTORS, CANNABINOID; TIME-LAPSE IMAGING;

EID: 79952771931     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5483-10.2011     Document Type: Article

References (72)

1. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzmán M, Galve-Roperh I (2005) The endocannabinoid system drives neural progenitor proliferation. FASEB J 19:1704-1706. (Pubitemid 41429536)
2. Alvarez-Buylla A, Herrera DG, Wichterle H (2000) The subventricular zone: source of neuronal precursors for brain repair. Prog Brain Res 127:1-11. (Pubitemid 35461253)
3. Anton ES, Ghashghaei HT, Weber JL, McCann C, Fischer TM, Cheung ID, Gassmann M, Messing A, Klein R, Schwab MH, Lloyd KC, Lai C (2004) Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci 7:1319-1328. (Pubitemid 41057754)
4. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970. (Pubitemid 35033700)
5. Battista D, Rutishauser U (2010) Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues. J Neurosci 30:3995-4003.
6. Berghuis P, Dobszay MB, Wang X, Spano S, Ledda F, Sousa KM, Schulte G, Ernfors P, Mackie K, Paratcha G, Hurd YL, Harkany T (2005) Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc Natl Acad Sci U S A 102:19115-19120. (Pubitemid 43049575)
7. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463-468. (Pubitemid 37429860)
8. Blankman JL, Simon GM, Cravatt BF (2007) Acomprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 14:1347-1356. (Pubitemid 350257008)
9. Blázquez C, Casanova ML, Planas A, Gómez Del Pulgar T, Villanueva C, Fernández-Aceñero MJ, Aragonés J, Huffman JW, Jorcano JL, Guzmán M (2003) Inhibition of tumor angiogenesis by cannabinoids. FASEB J 17:529-531.
10. Boutin C, Diestel S, Desoeuvre A, Tiveron MC, Cremer H (2008) Efficient in vivo electroporation of the postnatal rodent forebrain. PLoS One 3:e1883.
11. Bovetti S, Bovolin P, Perroteau I, Puche AC (2007) Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur J Neurosci 25:2021-2033. (Pubitemid 46581726)
12. Bridges D, Rice AS, Egertová M, Elphick MR, Winter J, Michael GJ (2003) Localisation of cannabinoid receptor 1 in rat dorsal root ganglion using in situ hybridisation and immunohistochemistry. Neuroscience 119:803-812. (Pubitemid 36694807)
13. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10. (Pubitemid 37339753)
14. Chiaramello S, Dalmasso G, Bezin L, Marcel D, Jourdan F, Peretto P, Fasolo A, De Marchis S (2007) BDNF/ TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci 26:1780-1790. (Pubitemid 47493201)
15. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3:1091-1097.
16. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A (2005) Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283.
17. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949. (Pubitemid 23026736)
18. Diefenbach TJ, Latham VM, Yimlamai D, Liu CA, Herman IM, Jay DG (2002) Myosin 1c and myosin IIB serve opposing roles in lamellipodial dynamics of the neuronal growth cone. J Cell Biol 158:1207-1217.
19. Doherty P, Cohen J, Walsh FS (1990) Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 5:209-219. (Pubitemid 20262699)
20. Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489-498. (Pubitemid 32786992)
21. Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA, Doherty P (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30:2017-2024.
22. Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S (2008) Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci 28:5901-5909.
23. Goings GE, Sahni V, Szele FG (2004) Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res 996:213-226. (Pubitemid 38022018)
24. Goncalves MB, Suetterlin P, Yip P, Molina-Holgado F, Walker DJ, Oudin MJ, Zentar MP, Pollard S, Yáñez-Muñoz RJ, Williams G, Walsh FS, Pangalos MN, Doherty P (2008) A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol Cell Neurosci 38:526-536.
25. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, Uhl GR (2006) Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 1071:10-23. (Pubitemid 43255471)
26. Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH (2003) Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci 6:1284-1291. (Pubitemid 37485122)
27. Hoover HS, Blankman JL, Niessen S, Cravatt BF (2008) Selectivity of inhibitors of endocannabinoid biosynthesis evaluated by activity-based protein profiling. Bioorg Med Chem Lett 18:5838-5841.
28. Hu H, Tomasiewicz H, Magnuson T, Rutishauser U (1996) The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16:735-743. (Pubitemid 26124051)
29. Huang C (2010) Roles of E3 ubiquitin ligases in cell adhesion and migration. Cell Adh Migr 4:10-18.
30. Hurtado-Chong A, Yusta-Boyo MJ, Vergaño-Vera E, Bulfone A, de Pablo F, Vicario-Abejón C (2009) IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci 30:742-755.
31. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269. (Pubitemid 41740635)
32. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, Zhang X (2005) Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic-and antidepressant-like effects. J Clin Invest 115:3104-3116. (Pubitemid 41567575)
33. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, Childs J, Greenberg DA (2004) Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 66:204-208. (Pubitemid 38989476)
34. Jordà MA, Verbakel SE, Valk PJ, Vankan-Berkhoudt YV, Maccarrone M, Finazzi-Agrò A, Löwenberg B, Delwel R (2002) Hematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol. Blood 99:2786-2793. (Pubitemid 34525366)
35. Joseph J, Niggemann B, Zaenker KS, Entschladen F (2004) Anandamide is an endogenous inhibitor for the migration of tumor cells and T lymphocytes. Cancer Immunol Immunother 53:723-728. (Pubitemid 38962066)
36. Kappeler C, Saillour Y, Baudoin JP, Tuy FP, Alvarez C, Houbron C, Gaspar P, Hamard G, Chelly J, Métin C, Francis F (2006) Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum Mol Genet 15:1387-1400.
37. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105. (Pubitemid 34202283)
38. Keimpema E, Barabas K, Morozov YM, Tortoriello G, Torii M, Cameron G, Yanagawa Y, Watanabe M, Mackie K, Harkany T (2010) Differential subcellular recruitment of monoacylglycerol lipase generates spatial specificity of 2-arachidonoyl glycerol signaling during axonal pathfinding. J Neurosci 30:13992-14007.
39. Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG (2006) Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 9:779-786.
40. Kokaia Z, Thored P, Arvidsson A, Lindvall O (2006) Regulation of stroke-induced neurogenesis in adult brain - recent scientific progress. Cereb Cortex 16 [Suppl 1]:i162-i167.
41. Lois C, García-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978-981. (Pubitemid 26066393)
42. Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, Schlosburg JE, Pavón FJ, Serrano AM, Selley DE, Parsons LH, Lichtman AH, Cravatt BF (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 5:37-44.
43. Lunn CA, Fine JS, Rojas-Triana A, Jackson JV, Fan X, Kung TT, Gonsiorek W, Schwarz MA, Lavey B, Kozlowski JA, Narula SK, Lundell DJ, Hipkin RW, Bober LA (2006) Anovel cannabinoid peripheral cannabinoid receptor-selective inverse agonist blocks leukocyte recruitment in vivo. J Pharmacol Exp Ther 316:780-788. (Pubitemid 43131006)
44. Maison P, Walker DJ, Walsh FS, Williams G, Doherty P (2009) BDNF regulates neuronal sensitivity to endocannabinoids. Neurosci Lett 467:90-94.
45. Marín O, Valiente M, Ge X, Tsai LH (2010) Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol 2:a001834.
46. Mechoulam R, Shohami E (2007) Endocannabinoids and traumatic brain injury. Mol Neurobiol 36:68-74. (Pubitemid 351360359)
47. Miller AM, Stella N (2008) CB2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 153:299-308.
48. Mulder J, Aguado T, Keimpema E, Barabás K, Ballester Rosado CJ, Nguyen L, Monory K, Marsicano G, Di Marzo V, Hurd YL, Guillemot F, Mackie K, Lutz B, Guzmán M, Lu HC, Galve-Roperh I, Harkany T (2008) Endocannabinoid signaling controls pyramidal cell specification and longrange axon patterning. Proc Natl Acad Sci U S A 105:8760-8765. (Pubitemid 351987753)
49. Murase S, Cho C, White JM, Horwitz AF (2008) ADAM2 promotes migration of neuroblasts in the rostral migratory stream to the olfactory bulb. Eur J Neurosci 27:1585-1595. (Pubitemid 351473570)
50. Nasrallah IM, McManus MF, Pancoast MM, Wynshaw-Boris A, Golden JA (2006) Analysis of non-radial interneuron migration dynamics and its disruption in Lis1+/- mice. J Comp Neurol 496:847-858.
51. Ono K, Tomasiewicz H, Magnuson T, Rutishauser U (1994) N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13:595-609.
52. Ortar G, Bisogno T, Ligresti A, Morera E, Nalli M, Di Marzo V (2008) Tetrahydrolipstatin analogues as modulators of endocannabinoid 2-arachidonoylglycerol metabolism. J Med Chem 51:6970-6979.
53. Palazuelos J, Aguado T, Egia A, Mechoulam R, Guzmán M, Galve-Roperh I (2006) Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 20:2405-2407.
54. Paratcha G, Ibáñez CF, Ledda F (2006) GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream. Mol Cell Neurosci 31:505-514. (Pubitemid 43361927)
55. Patinkin, D, Milman, G, Breuer, A, Fride, E, Mechoulam, R (2008) Endocannabinoids as positive or negative factors in hematopoietic cell migration and differentiation. Eur J Pharmacol 595:1-6.
56. Pertwee RG (2006) The pharmacology of cannabinoid receptors and their ligands: an overview. Int J Obes 30 [Suppl 1]:S13-S18.
57. Pollard SM, Conti L, Sun Y, Goffredo D, Smith A (2006) Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 16 [Suppl 1]:i112-i120.
58. Preet A, Ganju RK, Groopman JE (2008) Delta9-Tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene 27:339-346.
59. Rouzer, CA, Ghebreselasie, K, Marnett, LJ (2002) Chemical stability of 2-arachidonylglycerol under biological conditions. Chem Phys Lipids 119:69-82. (Pubitemid 35247918)
60. Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A 102:13652-13657. (Pubitemid 41420903)
61. Straiker A, Hu SS, Long JZ, Arnold A, Wager-Miller J, Cravatt BF, Mackie K (2009) Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Molecular pharmacology 76:1220-1227.
62. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174. (Pubitemid 24015289)
63. Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N-and P/Qtype calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78:43-50. (Pubitemid 27318909)
64. Ward ME, Rao Y (2005b) Investigations of neuronal migration in the central nervous system. Methods Mol Biol 294:137-156.
65. Ward ME, Jiang H, Rao Y (2005a) Regulated formation and selection of neuronal processes underlie directional guidance of neuronal migration. Mol Cell Neurosci 30:378-387. (Pubitemid 41417781)
66. Wichterle H, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18:779-791. (Pubitemid 27232788)
67. Williams EJ, Walsh FS, Doherty P (2003) The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J Cell Biol 160:481-486. (Pubitemid 36254386)
68. Witting A, Chen L, Cudaback E, Straiker A, Walter L, Rickman B, Möller T, Brosnan C, Stella N (2006) Experimental autoimmune encephalomyelitis disrupts endocannabinoid-mediated neuroprotection. Proc Natl Acad Sci U S A 103:6362-6367.
69. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M (2006) Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751. (Pubitemid 44315313)
70. Zhang H, Vutskits L, Pepper MS, Kiss JZ (2003) VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163:1375-1384. (Pubitemid 38032097)
71. Zhang RL, LeTourneau Y, Gregg SR, Wang Y, Toh Y, Robin AM, Zhang ZG, Chopp M (2007) Neuroblast division during migration toward the ischemic striatum: a study of dynamic migratory and proliferative characteristics of neuroblasts from the subventricular zone. J Neurosci 27:3157-3162. (Pubitemid 46474136)
72. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M (2004) Activated neural stem cells contribute to strokeinduced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24:441-448. (Pubitemid 38452235)